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Research article

Clinical Microbiology and Biomedical Sciences

Effect of Oral Administration of Lactobacillus plantarum HY7714 on Epidermal Hydration in Ultraviolet B-Irradiated Hairless Mice

Jehyeon Ra 1, Dong Eun Lee 1, Sung Hwan Kim 1, Ji-Woong Jeong 1, Hyung Keun Ku 1, Tae-Youl Kim 1, Il-Dong Choi 1, Woonhee Jeung 1, Jae-Hun Sim 1 and Young-Tae Ahn 1*

Korea Yakult Co., Ltd., Yongin 446-901, Republic of Korea

Received: August 11, 2014; Accepted: August 31, 2014

J. Microbiol. Biotechnol. 2014; 24(12): 1736-1743

Published December 28, 2014 https://doi.org/10.4014/jmb.1408.08023

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

In this study, we evaluated the effect of Lactobacillus plantarum HY7714 on skin hydration in human dermal fibroblasts and in hairless mice. In Hs68 cells, L. plantarum HY7714 not only increased the serine palmitoyltransferase (SPT) mRNA level, but also decreased the ceramidase mRNA level. In order to confirm the hydrating effects of L. plantarum HY7714 in vivo, we orally administered vehicle or L. plantarum HY7714 at a dose of 1 × 109 CFU/day to hairless mice for 8 weeks. In hairless mice, L. plantarum HY7714 decreased UVB-induced epidermal thickness. In addition, we found that L. plantarum HY7714 administration suppressed the increase in transepidermal water loss and decrease in skin hydration, which reflects barrier function fluctuations following UV irradiation. In particular, L. plantarum HY7714 administration increased the ceramide level compared with that in the UVB group. In the experiment on SPT and ceramidase mRNA expressions, L. plantarum HY7714 administration improved the reduction in SPT mRNA levels and suppressed the increase in ceramidase mRNA levels caused by UVB in the hairless mice skins. Collectively, these results suggest that L. plantarum HY7714 can be a potential candidate for preserving skin hydration levels against UV irradiation.

Keywords

Skin, Hydration, Lactobacillus plantarum HY7714, Serine palmitoyltransferase, ceramidase, ceramide

References

  1. Arck P, Handjiski B, Hagen E, Pincus M, Bruenahl C, Bienenstock J, et al. 2010. Is there a ‘gut-brain-skin axis’? Exp. Dermatol. 19: 410-405.
    Pubmed CrossRef
  2. Arikawa J, Ishibashi M, Kawashima M, Takagi Y, Ichikawa Y, Imokawa G. 2002. Decreased levels of sphingosine, a natural antimicrobial agent, may be associated with vulnerability of the stratum corneum from patients with atopic dermatitis to colonization by Staphylococcus aureus. J. Investig. Dermatol. 119: 433-439.
    Pubmed CrossRef
  3. Armstrong BK, Kricker A. 2001. The epidemiology of UV induced skin cancer. J. Photochem. Photobiol. B 63: 8-18.
    CrossRef
  4. Baba H, Masuyama A, Yoshimura C, Aoyama Y, Takano T, Ohki K. 2010. Oral intake of Lactobacillus helveticus-fermented milk whey decreased transepidermal water loss and prevented the onset of sodium dodecylsulfate-induced dermatitis in mice. Biosci. Biotechnol. Biochem. 74: 18-23.
    Pubmed CrossRef
  5. Barel AO, Clarys P. 1995. Study of the stratum corneum barrier function by transepidermal water loss measurements:comparison between two commercial instruments: Evaporimeter and Tewameter. Skin. Pharmacol. 8: 186-195.
    CrossRef
  6. Bouilly-Gauthier D, Jeannes C, Maubert Y, Duteil L, QueilleRoussel C, Piccardi N, et al. 2010. Clinical evidence of benefits of a dietary supplement containing probiotic and carotenoids on ultraviolet-induced skin damage. Br. J. Dermatol. 163:536-543.
    Pubmed CrossRef
  7. Blichmann CW, Serup J. 1998. Assessment of skin moisture. Measurement of electrical conductance, capacitance and transepidermal water loss. Acta. Derm. Venereol. 68: 284-290.
  8. Elias PM, Menon GK. 1991. Structural and lipid biochemical correlates of the epidermal permeability barrier. Adv. Lipid Res. 24: 1-26.
    Pubmed CrossRef
  9. FAO/WHO. 2001. Guidelines for the evaluation of probiotics in food (probiotic_guidelines.pdf, editor). London/Ontario:FAO/WHO.
  10. Farkas B, Magyarlaki M, Csete B, Nemeth J, Rabloczky G, Bernath S, et al. 2002. Reduction of acute photodamage in skin by topical application of a novel PARP inhibitor. Biochem. Pharmacol. 63: 921-932.
    CrossRef
  11. Farrll AM, Uchida Y, Nagiec MM, Harris IR, Dickson RC, Elias PM, et al. 1998. UVB irradiation up-regulates serine palmitoyl transferase in cultured human keratinocytes. J. Lipid Res. 39: 2031-2038.
  12. Fuchs J. 1998. Potentials and limitations of the natural antioxidants RRR-α-tocopherol, L-ascorbic acid and β-carotene in cutaneous photoprotection. Free Radic. Biol. Med. 25: 848-873.
    CrossRef
  13. Guéniche A, Benyacoub J, Blum S, Breton L, Castiel I. 2009. Probiotics for skin benefits, pp. 421-439. In Tabor A, Blair R (eds.). Nutritional cosmetics: beauty from within. Elsevier, Oxford.
    CrossRef
  14. Holleran WM, Uchida Y, Halkier-Sorensen L, Haratake A, Hara M, Epstein JH, et al. 1997. Structural and biochemical basis for the UVB-induced alterations in epidermal barrier function. Photodermatol. Photoimmunol. Photomed. 13: 117-128.
    Pubmed CrossRef
  15. Hougee S, Vriesema AJ, Wijering SC, Knippels LM, Folkerts G, Nijkamp, et al. 2010. Oral treatment with probiotics reduces allergic symptoms in ovalbumin-sensitized mice: a bacterial strain comparative study. Int. Arch. Allergy Immunol. 151: 107-117.
    Pubmed CrossRef
  16. Iizuka R, Kawakami K, Izawa N, Chiba K. 2009. Phenols produced by gut bacteria affect the skin in hairless mice. Microb. Ecol. Health Dis. 21: 50-56.
    CrossRef
  17. Kim H, Oh I, Park KH, Kim NM, Do JH, Cho Y. 2009. Stimulatory effect of dietary red ginseng on epidermal hydration and ceramide levels in ultraviolet-irradiated hairless mice. J. Med. Food 12: 746-754.
    Pubmed CrossRef
  18. Kim HJ, Kim YJ, Kang MJ, Seo JH, Kim HY, Jeong SK, et al. 2012. A novel mouse model of atopic dermatitis with epicutaneous allergen sensitization and the effect of Lactobacillus rhamnosus. Exp. Dermatol. 21: 672-675.
    Pubmed CrossRef
  19. Kim H, Oh I, Park KH, Kim NM, Do JH, Cho Y. 2009. Stimulatory effect of dietary red ginseng on epidermal hydration and ceramide levels in ultraviolet-irradiated hairless mice. J. Med. Food. 12: 746-754.
    Pubmed CrossRef
  20. Kleerebezem M, Hols P, Bernard E, Rolain T, Zhou M, Siezen RJ, et al. 2010. The extracellular biology of the lactobacilli. FEMS Microbiol. Rev. 34: 199-230.
    Pubmed CrossRef
  21. Krutmann J. 2009. Pre- and probiotics for human skin. J. Dermatol. Sci. 54: 1-5.
    Pubmed CrossRef
  22. Liu K, Yu D, Cho YY, Bode AM, Ma W, Yao K, et al. 2013. Sunlight UV-induced skin cancer relies upon activation of the p38a signaling pathway. Cancer Res. 73: 2181-2188.
    Pubmed CrossRef
  23. Magnoni C, Euclidi E, Benassi L, Bertazzoni G, Cossarizza A, Seidenari S, et al. 2002. Ultraviolet B irradiation induces activation of neutral and acidic sphingomyelinases and ceramide generation in cultured normal human keratinocytes. Toxicol. In Vitro 16: 349-355.
    CrossRef
  24. Marteau P, Boutron-Ruault MC. 2002. Nutritional advantages of probiotics and prebiotics. Br. J. Nutr. 87(Suppl 2): S153S157.
  25. Meguro S, Arai Y, Masukawa K, Uie K, Tokimitsu I. 1999. Stratum corneum lipid abnormalities in UVB-irradiated skin. Photochem. Photobiol. 69: 317-321.
    CrossRef
  26. Morganti P. 2009. The photoprotective activity of nutraceuticals. Clin. Dermatol. 27: 166-174.
    Pubmed CrossRef
  27. Park KH, Choi YS, Kim H, Lee KG, Yeo JH, Jung DH, et al. 2007. Dietary effect of silk protein on ceramide synthesis and the expression of ceramide metabolic enzymes in the epidermis of NC/Nga mice. J. Korean. Soc. Food. Sci. Nutr. 36: 554-562.
  28. Paz M L , González M aglio DH, W eill F S, B ustamante J, Leoni J. 2008. Mitochondrial dysfunction and cellular stress progression after ultraviolet B irradiation in human keratinocytes. Photodermatol. Photoimmunol. Photomed. 24: 115-122.
    Pubmed CrossRef
  29. Pyun HB, Kim M, Park J, Sakai Y, Numata N, Shin JY, et al. 2012. Effects of collagen tripeptide supplement on photoaging and epidermal skin barrier in UVB-exposed hairless mice. Prev. Nutr. Food Sci. 17: 245–253.
    Pubmed CrossRef
  30. Rabionet M, Gorgas K, Sandhoff R. 2014. Ceramide synthesis in the epidermis. Biochim. Biophys. Acta 1841: 422-434.
    Pubmed CrossRef
  31. Song J, Liu P, Yang Z, Li L, Su H, Lu N, et al. 2012. MiR-155 negatively regulates c-jun expression at the post-transcriptional level in human dermal fibroblasts in vitro: implications in UVA irradiation-induced photoaging. Cell Physiol. Biochem. 29: 331-340.
    Pubmed CrossRef
  32. Sugimoto S, Ishii Y, Izawa N, Masuoka N, Kano M, Sone T, et al. 2012. Photoprotective effects of Bifidobacterium breve supplementation against skin damage induced by ultraviolet irradiation in hairless mice. Photodermatol. Photoimmunol. Photomed. 28: 312–319.
    Pubmed CrossRef
  33. Svobodova A, Walterova D, Vostalova J. 2006. Ultraviolet light induced alteration to the skin. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 150: 25-38.
    Pubmed CrossRef
  34. Takagi Y, Nagagawa H, Kondo H, Takema Y, Imokawa G. 2004. Decreased levels of covalently bound ceramide are associated with ultraviolet B-induced perturbation of the skin barrier. J. Invest. Dermatol. 106: 59-63.
  35. Takino Y, Okura F, Kitazawa M, Iwasaki K, Tagami H. 2012. Zinc L-pyrrolidone carboxylate inhibits the UVAinduced production of matrix metalloproteinase-1 by in vitro cultured skin fibroblasts, whereas it enhances their collagen synthesis. Int. J. Cosmetic Sci. 34: 23-28.
    Pubmed CrossRef
  36. Tang ML, Lahtiner SJ, Boyle RJ. 2010. Probiotics and prebiotics:clinical effects in allergic disease. Curr. Opin. Pediatr. 22:626-634.
    Pubmed
  37. Wang H, Kochevar IE. 2005. Involvement of UBV-induced reactive oxygen species in TGF-beta biosynthesis and activation in keratinocytes. Free Radic. Biol. Med. 38: 890-897.
    Pubmed CrossRef
  38. You GE, Jung BJ, Kim HR, Kim HG, Kim TR, Chung DK. 2013. Lactobacillus sakei lipoteichoic acid inhibits MMP-1 induced by UVA in normal dermal fibroblasts of human. J. Microbiol. Biotechnol. 23: 1357–1364.
    Pubmed CrossRef
  39. Zuo Y, Zhuang DZ, Han R, Isaac G, Tobin JJ, McKee M, et al. 2008. ABCA12 maintains the epidermal lipid permeability barrier by facilitating formation of ceramide linoleic esters. J. Biol. Chem. 283: 36624-36635.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2014; 24(12): 1736-1743

Published online December 28, 2014 https://doi.org/10.4014/jmb.1408.08023

Copyright © The Korean Society for Microbiology and Biotechnology.

Effect of Oral Administration of Lactobacillus plantarum HY7714 on Epidermal Hydration in Ultraviolet B-Irradiated Hairless Mice

Jehyeon Ra 1, Dong Eun Lee 1, Sung Hwan Kim 1, Ji-Woong Jeong 1, Hyung Keun Ku 1, Tae-Youl Kim 1, Il-Dong Choi 1, Woonhee Jeung 1, Jae-Hun Sim 1 and Young-Tae Ahn 1*

Korea Yakult Co., Ltd., Yongin 446-901, Republic of Korea

Received: August 11, 2014; Accepted: August 31, 2014

Abstract

In this study, we evaluated the effect of Lactobacillus plantarum HY7714 on skin hydration in
human dermal fibroblasts and in hairless mice. In Hs68 cells, L. plantarum HY7714 not only
increased the serine palmitoyltransferase (SPT) mRNA level, but also decreased the
ceramidase mRNA level. In order to confirm the hydrating effects of L. plantarum HY7714 in
vivo, we orally administered vehicle or L. plantarum HY7714 at a dose of 1 × 109 CFU/day to
hairless mice for 8 weeks. In hairless mice, L. plantarum HY7714 decreased UVB-induced
epidermal thickness. In addition, we found that L. plantarum HY7714 administration
suppressed the increase in transepidermal water loss and decrease in skin hydration, which
reflects barrier function fluctuations following UV irradiation. In particular, L. plantarum
HY7714 administration increased the ceramide level compared with that in the UVB group. In
the experiment on SPT and ceramidase mRNA expressions, L. plantarum HY7714
administration improved the reduction in SPT mRNA levels and suppressed the increase in
ceramidase mRNA levels caused by UVB in the hairless mice skins. Collectively, these results
suggest that L. plantarum HY7714 can be a potential candidate for preserving skin hydration
levels against UV irradiation.

Keywords: Skin, Hydration, Lactobacillus plantarum HY7714, Serine palmitoyltransferase, ceramidase, ceramide

References

  1. Arck P, Handjiski B, Hagen E, Pincus M, Bruenahl C, Bienenstock J, et al. 2010. Is there a ‘gut-brain-skin axis’? Exp. Dermatol. 19: 410-405.
    Pubmed CrossRef
  2. Arikawa J, Ishibashi M, Kawashima M, Takagi Y, Ichikawa Y, Imokawa G. 2002. Decreased levels of sphingosine, a natural antimicrobial agent, may be associated with vulnerability of the stratum corneum from patients with atopic dermatitis to colonization by Staphylococcus aureus. J. Investig. Dermatol. 119: 433-439.
    Pubmed CrossRef
  3. Armstrong BK, Kricker A. 2001. The epidemiology of UV induced skin cancer. J. Photochem. Photobiol. B 63: 8-18.
    CrossRef
  4. Baba H, Masuyama A, Yoshimura C, Aoyama Y, Takano T, Ohki K. 2010. Oral intake of Lactobacillus helveticus-fermented milk whey decreased transepidermal water loss and prevented the onset of sodium dodecylsulfate-induced dermatitis in mice. Biosci. Biotechnol. Biochem. 74: 18-23.
    Pubmed CrossRef
  5. Barel AO, Clarys P. 1995. Study of the stratum corneum barrier function by transepidermal water loss measurements:comparison between two commercial instruments: Evaporimeter and Tewameter. Skin. Pharmacol. 8: 186-195.
    CrossRef
  6. Bouilly-Gauthier D, Jeannes C, Maubert Y, Duteil L, QueilleRoussel C, Piccardi N, et al. 2010. Clinical evidence of benefits of a dietary supplement containing probiotic and carotenoids on ultraviolet-induced skin damage. Br. J. Dermatol. 163:536-543.
    Pubmed CrossRef
  7. Blichmann CW, Serup J. 1998. Assessment of skin moisture. Measurement of electrical conductance, capacitance and transepidermal water loss. Acta. Derm. Venereol. 68: 284-290.
  8. Elias PM, Menon GK. 1991. Structural and lipid biochemical correlates of the epidermal permeability barrier. Adv. Lipid Res. 24: 1-26.
    Pubmed CrossRef
  9. FAO/WHO. 2001. Guidelines for the evaluation of probiotics in food (probiotic_guidelines.pdf, editor). London/Ontario:FAO/WHO.
  10. Farkas B, Magyarlaki M, Csete B, Nemeth J, Rabloczky G, Bernath S, et al. 2002. Reduction of acute photodamage in skin by topical application of a novel PARP inhibitor. Biochem. Pharmacol. 63: 921-932.
    CrossRef
  11. Farrll AM, Uchida Y, Nagiec MM, Harris IR, Dickson RC, Elias PM, et al. 1998. UVB irradiation up-regulates serine palmitoyl transferase in cultured human keratinocytes. J. Lipid Res. 39: 2031-2038.
  12. Fuchs J. 1998. Potentials and limitations of the natural antioxidants RRR-α-tocopherol, L-ascorbic acid and β-carotene in cutaneous photoprotection. Free Radic. Biol. Med. 25: 848-873.
    CrossRef
  13. Guéniche A, Benyacoub J, Blum S, Breton L, Castiel I. 2009. Probiotics for skin benefits, pp. 421-439. In Tabor A, Blair R (eds.). Nutritional cosmetics: beauty from within. Elsevier, Oxford.
    CrossRef
  14. Holleran WM, Uchida Y, Halkier-Sorensen L, Haratake A, Hara M, Epstein JH, et al. 1997. Structural and biochemical basis for the UVB-induced alterations in epidermal barrier function. Photodermatol. Photoimmunol. Photomed. 13: 117-128.
    Pubmed CrossRef
  15. Hougee S, Vriesema AJ, Wijering SC, Knippels LM, Folkerts G, Nijkamp, et al. 2010. Oral treatment with probiotics reduces allergic symptoms in ovalbumin-sensitized mice: a bacterial strain comparative study. Int. Arch. Allergy Immunol. 151: 107-117.
    Pubmed CrossRef
  16. Iizuka R, Kawakami K, Izawa N, Chiba K. 2009. Phenols produced by gut bacteria affect the skin in hairless mice. Microb. Ecol. Health Dis. 21: 50-56.
    CrossRef
  17. Kim H, Oh I, Park KH, Kim NM, Do JH, Cho Y. 2009. Stimulatory effect of dietary red ginseng on epidermal hydration and ceramide levels in ultraviolet-irradiated hairless mice. J. Med. Food 12: 746-754.
    Pubmed CrossRef
  18. Kim HJ, Kim YJ, Kang MJ, Seo JH, Kim HY, Jeong SK, et al. 2012. A novel mouse model of atopic dermatitis with epicutaneous allergen sensitization and the effect of Lactobacillus rhamnosus. Exp. Dermatol. 21: 672-675.
    Pubmed CrossRef
  19. Kim H, Oh I, Park KH, Kim NM, Do JH, Cho Y. 2009. Stimulatory effect of dietary red ginseng on epidermal hydration and ceramide levels in ultraviolet-irradiated hairless mice. J. Med. Food. 12: 746-754.
    Pubmed CrossRef
  20. Kleerebezem M, Hols P, Bernard E, Rolain T, Zhou M, Siezen RJ, et al. 2010. The extracellular biology of the lactobacilli. FEMS Microbiol. Rev. 34: 199-230.
    Pubmed CrossRef
  21. Krutmann J. 2009. Pre- and probiotics for human skin. J. Dermatol. Sci. 54: 1-5.
    Pubmed CrossRef
  22. Liu K, Yu D, Cho YY, Bode AM, Ma W, Yao K, et al. 2013. Sunlight UV-induced skin cancer relies upon activation of the p38a signaling pathway. Cancer Res. 73: 2181-2188.
    Pubmed CrossRef
  23. Magnoni C, Euclidi E, Benassi L, Bertazzoni G, Cossarizza A, Seidenari S, et al. 2002. Ultraviolet B irradiation induces activation of neutral and acidic sphingomyelinases and ceramide generation in cultured normal human keratinocytes. Toxicol. In Vitro 16: 349-355.
    CrossRef
  24. Marteau P, Boutron-Ruault MC. 2002. Nutritional advantages of probiotics and prebiotics. Br. J. Nutr. 87(Suppl 2): S153S157.
  25. Meguro S, Arai Y, Masukawa K, Uie K, Tokimitsu I. 1999. Stratum corneum lipid abnormalities in UVB-irradiated skin. Photochem. Photobiol. 69: 317-321.
    CrossRef
  26. Morganti P. 2009. The photoprotective activity of nutraceuticals. Clin. Dermatol. 27: 166-174.
    Pubmed CrossRef
  27. Park KH, Choi YS, Kim H, Lee KG, Yeo JH, Jung DH, et al. 2007. Dietary effect of silk protein on ceramide synthesis and the expression of ceramide metabolic enzymes in the epidermis of NC/Nga mice. J. Korean. Soc. Food. Sci. Nutr. 36: 554-562.
  28. Paz M L , González M aglio DH, W eill F S, B ustamante J, Leoni J. 2008. Mitochondrial dysfunction and cellular stress progression after ultraviolet B irradiation in human keratinocytes. Photodermatol. Photoimmunol. Photomed. 24: 115-122.
    Pubmed CrossRef
  29. Pyun HB, Kim M, Park J, Sakai Y, Numata N, Shin JY, et al. 2012. Effects of collagen tripeptide supplement on photoaging and epidermal skin barrier in UVB-exposed hairless mice. Prev. Nutr. Food Sci. 17: 245–253.
    Pubmed CrossRef
  30. Rabionet M, Gorgas K, Sandhoff R. 2014. Ceramide synthesis in the epidermis. Biochim. Biophys. Acta 1841: 422-434.
    Pubmed CrossRef
  31. Song J, Liu P, Yang Z, Li L, Su H, Lu N, et al. 2012. MiR-155 negatively regulates c-jun expression at the post-transcriptional level in human dermal fibroblasts in vitro: implications in UVA irradiation-induced photoaging. Cell Physiol. Biochem. 29: 331-340.
    Pubmed CrossRef
  32. Sugimoto S, Ishii Y, Izawa N, Masuoka N, Kano M, Sone T, et al. 2012. Photoprotective effects of Bifidobacterium breve supplementation against skin damage induced by ultraviolet irradiation in hairless mice. Photodermatol. Photoimmunol. Photomed. 28: 312–319.
    Pubmed CrossRef
  33. Svobodova A, Walterova D, Vostalova J. 2006. Ultraviolet light induced alteration to the skin. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 150: 25-38.
    Pubmed CrossRef
  34. Takagi Y, Nagagawa H, Kondo H, Takema Y, Imokawa G. 2004. Decreased levels of covalently bound ceramide are associated with ultraviolet B-induced perturbation of the skin barrier. J. Invest. Dermatol. 106: 59-63.
  35. Takino Y, Okura F, Kitazawa M, Iwasaki K, Tagami H. 2012. Zinc L-pyrrolidone carboxylate inhibits the UVAinduced production of matrix metalloproteinase-1 by in vitro cultured skin fibroblasts, whereas it enhances their collagen synthesis. Int. J. Cosmetic Sci. 34: 23-28.
    Pubmed CrossRef
  36. Tang ML, Lahtiner SJ, Boyle RJ. 2010. Probiotics and prebiotics:clinical effects in allergic disease. Curr. Opin. Pediatr. 22:626-634.
    Pubmed
  37. Wang H, Kochevar IE. 2005. Involvement of UBV-induced reactive oxygen species in TGF-beta biosynthesis and activation in keratinocytes. Free Radic. Biol. Med. 38: 890-897.
    Pubmed CrossRef
  38. You GE, Jung BJ, Kim HR, Kim HG, Kim TR, Chung DK. 2013. Lactobacillus sakei lipoteichoic acid inhibits MMP-1 induced by UVA in normal dermal fibroblasts of human. J. Microbiol. Biotechnol. 23: 1357–1364.
    Pubmed CrossRef
  39. Zuo Y, Zhuang DZ, Han R, Isaac G, Tobin JJ, McKee M, et al. 2008. ABCA12 maintains the epidermal lipid permeability barrier by facilitating formation of ceramide linoleic esters. J. Biol. Chem. 283: 36624-36635.
    Pubmed CrossRef